Classification of the “human tail”: Correlation between position, associated anomalies, and causes Sayaka Tojima, Shigehito Yamada Citation Clinical Anatomy. 33(6); 929-942. Issue Date 2020-09 Version of Record 2020-06-04 Type Journal article Textversion Author This is the pre-peer reviewed version of the following article: Clinical Anatomy. Vol.33, Issu.6, p.929-942., which has been published in final form at Rights https://doi.org/10.1002/ca.23609. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions. DOI 10.1002/ca.23609 Self-Archiving by Author(s) Placed on: Osaka City University Repository TOJIMA, S., & YAMADA, S. (2020). Classification of the "human tail": Correlation between position, associated anomalies, and causes. Clinical Anatomy. 33, 929-942. DOI:10.1002/ca.23609. Title: Classification of the “human tail”: correlation between position, associated anomalies, and causes Abstract Introduction: Numerous case reports have indicated that the “human tail” is not always a harmless protrusion but can be associated with anomalies such as occult dysraphic malformations. However, the definition and classification of this anomaly have not been discussed. A prevailing hypothesis is that the “human tail” is a residual embryonic tail. Herein, we attempted to classify and define the human tail and investigate the frequency of this anomaly. Materials and Methods: We first defined the human tail as a protrusion on the dorsal side of the lumbar, sacrococcygeal, and para-anal regions identified after birth. We collected case reports written in English, Japanese, French, German, and Italian that were published from the 1880s to the present. Results: We discovered two important findings: (1) the cause of this anomaly may differ even though the “tails” resemble each other closely in appearance, and (2) its position tends to be correlated with the type of anomaly and its associated cause. We propose a new classification of the human tail based on these findings. Conclusions: Our classification may facilitate more accurate treatment and precise case descriptions of the human tail. Keywords: tail, congenital anomalies, spina bifida, diagnosis 1 INTRODUCTION In vertebrates, a tail is generally defined as an elongated trunk posterior to the anus (or the cloaca). It contains musculoskeletal elements (caudal vertebrae and muscles) and neurovascular tissues providing innervation to the muscles. Naturally, a tail is relatively mobile. The caudal vertebrae are part of the skeletal system that maintains the tail, which articulates posterior to the sacrum (Tojima, 2013). Tails in vertebrates present as various morphological types and possess numerous roles. Humans still have a coccyx, which is homologous to the caudal vertebrae; however, it is typically curved anteriorly and does not protrude externally. Extant hominoids (so-called apes), including humans, have lost their tails completely. The tail reduction process during evolution remains a mystery due to incomplete fossil records. At present, studies have clearly demonstrated that our ancestors lost their tails at some point during a 20-million-year period between the Oligocene and Miocene epochs. Unfortunately, no fossils connecting these ancestral species have ever been found (Fleagle, 2012; Ward et al., 1991; Nakatsukasa et al., 2003, 2004). Human embryos have temporary tails, in which somites exist up to the tip of the tail. The number of caudal somites gradually increases by 8 weeks of pregnancy (Carnegie Stage [CS] 16). Just two days after the number peaks (CS17), it abruptly decreases by almost five pairs of somites (Tojima et al., 2018). Thus, human embryonic tail reduction is caused by an abrupt and dynamic decrease in the number of somites, which would have become the caudal vertebrae. Apoptosis is a possible cellular mechanism underpinning this phenomenon. A previous study reported an increase in macrophages at the tip of the embryonic tail and suggested that cell death may be related to embryonic tail reduction (Fallon & Simandl, 2 1978). Clinically, the “human tail” is a congenital anomaly reported sporadically in case reports. As shown in Fig. 1, the shape, size, and location of this anomaly vary greatly. Several studies have attempted to classify it based on morphological differences and contents (Fig. 1, Table 1). However, since this anomaly is not fatal, its origins were considered unimportant. Thus, most classifications of this anomaly are not helpful to clinicians, and a definition of “human tail” has not been established. This has led to various anomalies being reported as “human tails.” Several types of classification of the “human tail” have been proposed since Bartles first classified this anomaly from a medical point of view (Table 1). In 1901, Harrison classified the “human tail” into two types (Harrison, 1901): the true tail (containing vertebrae) and the caudal appendage (no vertebrae). Subsequently, Giroud (1966) proposed another classification that was similar to Harrison’s classification. However, Dao and Netsky proposed a different classification in 1984, wherein they classified the human tail into a true tail and a pseudotail. According to their definitions, the true tail is a residual of the embryonic tail and does not contain any vertebrae, whereas the pseudotail is a caudal protrusion containing other normal or abnormal tissues (Dao & Netsky, 1984). The terms “true tail” and “pseudotail,” which were used in both Harrison’s and Dao and Netsky’s classifications, became widespread and have since been used in many reports. However, this terminology has made the definitions and classification inconsistent, because these two classifications were completely opposite with respect to the presence of vertebrae. Thus, the classification and definition of the anomaly have been inconsistent, particularly since the 1980s. A novel and clinically relevant definition and classification system is a critical unmet need. In this study, we attempted to classify, define, and investigate the 3 frequency of this anomaly. MATERIALS AND METHODS Among clinicians, a postero-dorsal protrusion tends to be reported as a “tail.” Thus, we defined the “human tail” as a protrusion on the dorsal side of the lumbar, sacrococcygeal, and para-anal regions found after birth. In this study, we also defined “sacrococcygeal” as the region below the iliac crest and above the natal cleft regions. This definition relied on the surface anatomy in order to incorporate previous reports without radiography or computed tomography (CT) observations. We collected case reports written in English, Japanese, French, German, and Italian that were published from the 1880s to the present. Case reports that did not meet the definition were excluded; for example, cases with caudal tenderness or pain caused by an insufficiently curved coccyx without an external protrusion (Bar-Maor et al., 1980; Hamoud, 2011; Zimmer and Bronshtein, 1996) or cases with a tail-like structure in the cervical region or upper limb (Gaskill and Marlin, 1989; Mohindra, 2007). We summarized the information from the collected case reports focusing on sex, location (vertebral and lateral levels), contents, and associated anomalies. Their tendencies were investigated. RESULTS A total of 195 cases were identified, and we summarized the information in Supplementary Table 1. The number of cases reported in Japanese from 1941 to 2016 was 95 (68 articles). The number of cases reported in English from 1881 to 2017 was 97 (60 articles), and the patients’ nationalities varied (e.g., USA, UK, Canada, India, Israel, Turkey, Japan, 4 China, etc.). Sex and age Among 195 cases, 84 male patients and 79 female patients had the anomaly (Table 2). The frequency of the anomaly was not significantly different between sexes (chi-square test, p>0.05). Except for 20 cases where patients were older than 11 years and five cases without information on age, most cases were reported in neonates and infants (Supplementary Table 1). This is simply due to the ease of identifying this anomaly and parents being eager to eliminate the “tail” as soon as possible. Contents of the “tail” and its location Among 195 cases collected in this study, tails in 35 cases contained bony or cartilaginous elements (Table 2). Since palpation and radiography can easily confirm the presence of bone or cartilage, human tails with bones have frequently been reported (Miller, 1881). The bone inside the tail can be divided into two types: coccyx and non-coccyx. In most cases, the bony human tail is caused by a protrusion of the coccyx (26/35 cases). In these cases, the human tail tends to be small and semi-spherical (Nitta et al., 2010). When the coccyx protrudes and forms the “human tail,” the number of caudal vertebrae constituting the coccyx is normal (2–4 vertebrae), and there are no additional vertebrae. This type of human tail is likely observed on the midline at the sacrococcygeal level. Human tails with non-coccyx bony elements were rare (Table 2). In many cases of the non-coccyx human tail, bones and cartilaginous elements were present. These bones and/or 5 cartilages did not articulate with the sacrum or coccyx, and their locations were often far from the vertebral column. Thus, these bones and cartilage were not considered additional vertebrae. This type of human tail is also observed on the midline in the lumbar or sacrococcygeal region, cephalad with respect to the natal cleft. In contrast, the majority of the 195 cases collected in this study were boneless (132 cases, Table 2). Associated anomalies In most cases, the human tail was associated with anomalies. Among them, spinal dysraphism (including both skeletal and neural anomalies) were the most common, present in 80 cases (Table 3). Dysraphic spinal cord malformation was reported in 63 cases. Previously, spinal cord malformations have been classified in various ways. In this study, we referred to Raimond (1998) and the “Clinical guidelines for lower urinary tract dysfunction in patients with spina bifida,” which was presented in 2017 by the Japanese Continence Society and the Japanese Urological Association.